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Davis, C. C.

Publications and source records attributed to Davis, C. C..

At least 19 recordsLinked to original sources

Independent evolution of harmala alkaloids in medicinal Syrian rue and ayahuasca plants

Plants from distantly related lineages can produce identical neuroactive molecules, many of which have been independently adopted across human societies for their medicinal and cognition-altering effects. This phenomenon is exemplified by the traditional use of Syrian rue (Peganum harmala) and the ayahuasca vine (Banisteriopsis caapi) for medicine and ritual. Despite diverging over 100 million years ago and inhabiting different continents and climates, both plants synthesize harmala alkaloids (HAs), which inhibit human monoamine oxidase and exhibit diverse neuroactive effects. Here, we combine gene expression analyses, genomics, and enzyme characterization to elucidate HA biosynthesis for both Syrian rue and ayahuasca vine. We reveal multiple layers of biochemical and genetic convergence in these pathways, including independent duplication and neofunctionalization of an ancestral enzyme from serotonin biosynthesis, and lineage-specific repurposing of primary metabolic genes to generate a reactive precursor for alkaloid scaffold formation. Our study resolves biosynthetic routes to HAs in two medicinal plants and demonstrates convergent evolution of specialized metabolism at the levels of enzymes, pathways, and genomes.

biochemistry↗

Herbarium specimens reliably track plant phenological responses to climate change in understudied montane biomes

Long-term field observations typically are the "gold-standard" for inferences of phenological sensitivities in montane systems but are spatially limited. Herbarium specimens provide broader spatial coverage, but their utility to accurately capture montane phenology remains poorly known. We compared flowering phenology of 45 species inferred from herbarium specimens with comparable data from nearly 50 years of direct observations at the Rocky Mountain Biological Laboratory. Estimates of flowering time and phenological sensitivity to snow density were consistent between herbarium specimens and observations, but observations revealed secondary flowering peaks. Herbarium specimens additionally yielded shallower estimates of phenological sensitivity to spring temperature than did field observations. Across co-occurring species, "early" flowering individuals inferred from herbarium specimens, rather than the mean response across all individuals, may better approximate community-level phenological responses to temperature changes. We conclude that herbarium specimens are reliable resources for closing gaps in understanding phenological variation along elevational gradients of montane systems.

ecology↗

Bees attend primarily to costs, not benefits, to avoid exploitation by floral mimics

Animals are expected to weigh costs and benefits when making foraging decisions. Flowering plants often offer floral food rewards to pollinators, but also frequently deceive pollinators into visiting without providing rewards. Although floral mimicry, in which rewardless flowers mimic rewarding (model) flowers is common, it remains unclear whether pollinators evaluate the relative costs and benefits of visiting each. Using a signal detection theory (SDT) framework, we investigated how bumble bee decisions respond to experimental manipulations of costs and benefits within an intersexual floral mimicry system in which unrewarding female flowers imperfectly mimic pollen-rewarding male flowers (models). Using a fully factorial design, we increased the cost of visiting mimics (by adding quinine), increased the benefit of visiting models (by adding pollen), increased both simultaneously, and made no changes (control). As predicted by SDT, increasing mimic costs led to a conservative bias: bees made more correct rejections, but fewer correct detections. Contradicting SDT predictions, enhancing model reward did not elicit a liberal bias and decision performance remained unchanged. Our findings suggest that bees prioritize avoiding costly errors under uncertainty, even when this limits potential gains. Such conservative foraging decisions may help stabilize deceptive systems by allowing mimics to persist despite moderate costs.

animal behavior and cognition↗

A generative deep learning approach for global species distribution prediction

Anthropogenic pressures on biodiversity necessitate efficient and scalable methods to predict global species distributions. Current species distribution models (SDMs) face limitations with large-scale datasets, complex interspecies interactions, and data quality. Here, we introduce EcoVAE, an autoencoder-based generative model that integrates bioclimatic variables with georeferenced occurrences. The model is trained separately for plants, butterflies, and mammals to predict global distributions at both genus and species levels. EcoVAE achieves high precision and speed, outperforming traditional SDMs in spatial block cross-validation. Through unsupervised learning, it captures underlying distribution patterns and reveals species associations that align with known prey-predator relationships. Additionally, it evaluates global sampling efforts and interpolates distributions in data-limited regions, offering new applications for biodiversity exploration and monitoring.

ecology↗

Pleistocene glaciation advances the younger temporal dimension of species diversification in a major biodiversity hotspot

O_LIThe expansive Himalayan-Hengduan Mountains (HM) and Qinghai-Tibet Plateau (QTP) form a biodiversity hotspot imperiled by global change. The species diversity, resulting from myriad factors led to plant diversification from 10 million years ago till now. However, despite understanding speciation timing better, a lack of in-depth population-level studies and a dearth of organismal sampling among closely related species and populations leaves an incomplete view of diversification trends and biotic influences. C_LIO_LIWe delve into the complex factors influencing diversification through genomic and eco-morphological analysis within the Stellera chamaejasme L. complex, known for its significant floral diversity. C_LIO_LIOur results uncover four cryptic species, indicating a more recent and younger diversification period ([~]2.67-0.9 Mya), driven by Pleistocene glaciation and a complex set of interacting biotic factors. These factors prompted allopatric speciation and advocated cyclical warming-cooling episodes along latitudinal and altitudinal gradients throughout the Pleistocene. C_LIO_LIThe study emphasizes the existence of cryptic species within these mountains, broadening our understanding of species diversification to more recent than previously recognized. This novel perspective may reshape evolutionary paradigms in plant science. Additionally, it also brings to light concerns over future warmings possible impacts on alpine species distribution and speciation, underlining the urgency for increased conservation efforts. C_LI

evolutionary biology↗

Phenologically-informed species distribution models (SDMs) forecast less species loss and turnover versus standard SDMs

Species distribution models (SDMs) have been central for documenting the relationship between species geographic ranges and environmental conditions for more than two decades. However, the vast majority of SDMs rarely consider functional traits, such as phenology, which strongly affect species demography and fitness. Using >120,000 herbarium specimens representing 360 plant species across the eastern United States, we developed a novel "phenology-informed" SDM that integrates dynamic phenological responses to changing climates. Compared to standard SDMs based only on abiotic variables, our phenology-informed SDMs forecast significantly lower species habitat loss and less species turnover within communities under climate change. These results suggest that phenotypic plasticity or local adaptation in phenology may help many species adjust their ecological niches and persist in their habitats during periods of rapid environmental change. By modeling historical data that link phenology, climate, and species distributions, our findings reveal how species reproductive phenology mediates their geographic distributions along environmental gradients and affects regional biodiversity patterns in the face of future climate change. More importantly, our newly developed model also circumvents the need for mechanistic models that explicitly link traits to occurrences for each species, thus better facilitating the deployment of trait-based SDMs across unprecedented spatial and taxonomic scales.

ecology↗

Molecular analyses place the genus Keraunea outside Convolvulaceae

The genus Keraunea was recently described in the Convolvulaceae Juss. family. Two species are currently recognised, both from Brazil. Molecular sequence data using three commonly applied DNA markers (matK, rbcL and the nuclear ribosomal Internal Transcribed Spacer) show that neither species is correctly placed in Convolvulaceae but indicates that the type, K. brasiliensis, should be placed in Malpighiaceae despite several morphological anomalies. The second species, K. capixaba, should be placed in Ehretiaceae. Given the surprising nature of these results, further studies are recommended before formal reclassification of these two taxa is made.

evolutionary biology↗

Herbarium records provide reliable phenology estimates in the understudied tropics

Plant phenology has been shifting dramatically in response to climate change, a shift that may have significant and widespread ecological consequences. Of particular concern are tropical biomes, which represent the most biodiverse and imperiled regions of the world. However, compared to temperate floras, we know little about phenological responses of tropical plants because long-term observational datasets from the tropics are sparse. Herbarium specimens have greatly increased our phenological knowledge in temperate regions, but similar data have been underutilized in the tropics and their suitability for this purpose has not been broadly validated. Here, we compare phenological estimates derived from field observational data (i.e., plot surveys) and herbarium specimens at various spatial and taxonomic scales to determine whether specimens can provide accurate estimations of reproductive timing and its spatial variation. Here we demonstrate that phenological estimates from field observations and herbarium specimens coincide well. Fewer than 5% of the species exhibited significant differences between flowering periods inferred from field observations versus specimens regardless of spatial aggregation. In contrast to studies based on field records, herbarium specimens sampled much larger geographic and climatic ranges, as has been documented previously for temperate plants, and effectively captured phenological responses across varied environments. Herbarium specimens are verified to be a vital resource for closing the gap in our phenological knowledge of tropical systems. Tropical plant reproductive phenology inferred from herbarium records are widely congruent with field observations, suggesting that they can (and should) be used to investigate phenological variation and their associated environmental cues more broadly across tropical biomes.

ecology↗

Herbarium specimens reveal herbivory patterns across the genus Cucurbita

PREMISEQuantifying how closely related plant species differ in susceptibility to insect herbivory is important for our understanding of variation in plant-insect ecological interactions and evolutionary pressures on plant functional traits. However, empirically measuring in situ variation in herbivory over the entire geographic range where a plant-insect complex occurs is logistically difficult. Recently, new methods have been developed to use herbarium specimens to investigate patterns in plant-insect interactions across geographic areas, and during periods of accelerating anthropogenic change. Such investigations can provide insights into changes in herbivory intensity and phenology in plants that are of ecological and agricultural importance. METHODSHere, we analyze 274 pressed herbarium samples from all 14 species in the economically important plant genus Cucurbita (Cucurbitaceae) to investigate variation in herbivory damage. This collection is comprised of specimens of wild, undomesticated Cucurbita that were collected from across their native range in the Neotropics and subtropics, and Cucurbita cultivars that were collected from both within their native range and from locations where they have been introduced for agriculture in temperate Eastern North America. RESULTSWe find that herbivory is common on individuals of all Cucurbita species collected from throughout their geographic ranges; however, estimates of herbivory varied considerably among individuals, with greater damage observed in specimens collected from unmanaged habitat. We also find evidence that mesophytic species accrue more insect damage than xerophytic species. CONCLUSIONSOur study demonstrates that herbarium specimens are a useful resource for understanding ecological interactions between domesticated crop plants and co-evolved insect herbivores.

ecology↗

Intergenerational niche differentiation in filmy ferns (Hymenophyllaceae)

Desiccation tolerance was a key trait that allowed plants to colonize land. However, little is known about the transition from desiccation tolerant non-vascular plants to desiccation sensitive vascular ones. Filmy ferns (Hymenophyllaceae) represent a useful system to investigate how water-stress strategies differ between non-vascular and vascular stages within a single organism because they have vascularized sporophytes and nonvascular gametophytes that are each capable of varying degrees of desiccation tolerance. To explore this, we surveyed sporophytes and gametophytes of 19 species (22 taxa including varieties) of filmy ferns on Moorea (French Polynesia) and used chlorophyll fluorescence to measure desiccation tolerance and light responses. We conducted phylogenetically informed analyses to identify differences in physiology between life stages and growth habits. Gametophytes had similar or less desiccation tolerance (ability to recover from 2 d desiccation at -86 MPa) and lower photosynthetic optima (maximum electron transport rate of photosystem II and light level at 95% of that rate) than sporophytes. Epiphytes were more tolerant of desiccation than terrestrial species in both life stages. Despite their lack of greater physiological tolerances, gametophytes of several species occurred over a wider elevational range than conspecific sporophytes. Our results demonstrate that filmy fern gametophytes and sporophytes differ in their physiology and niche requirements, and point to the importance of microhabitat in shaping the evolution of water-use strategies in vascular plants.

ecology↗

Back to the future: a refined single user photostation for massively scaling herbarium digitization

The digitization and online mobilization of herbarium specimens has greatly facilitated their access and helped ignite a revolution in the biodiversity sciences (Drew et al., 2017; Hedrick et al., 2020; Nelson et al., 2015; Soltis, 2017; Sweeney et al., 2018; Thiers et al., 2016). These efforts have mobilized millions of specimens with significant economies of scale and accelerated advances in scientific investigations, including phenological studies of climate change, species range assessments, and biotic interactions (Hedrick et al., 2020; Meineke et al., 2019; Meineke et al., 2018; Pearson et al., 2020; Willis et al., 2017). In addition, the use of natural history collections to answer scientific questions using only their digitized representation, rather than the physical specimen itself-i.e., Digitization 2.0 sensu Hedrick et al. (2020)-has sparked the integration and development of new scholarly disciplines and lines of inquiry not previously possible. Despite these exciting new directions, however, Digitization 1.0 sensu Hedrick et al. (2020)-i.e., the generation of digitized products from the physical specimen-remains an active area of innovation and development. This relates to both hardware and workflow innovations as well as their integration with advancements in software. Along these lines, innovations in these areas have greatly increased the cost-effectiveness of digitizing herbarium specimens and enabled the successful mobilization of entire collections and whole floristic regions (Heerlien et al., 2015; Pignal and Michiels, 2012; Schorn et al., 2016; Slijkhuis, 2014; Sweeney et al., 2018; van Oever and Gofferje, 2012). Here, we present a novel photostation and workstation design for imaging herbarium specimen that represents a dramatic improvement upon existing approaches and is scalable for large and small institutions alike.

plant biology↗

Response to Kozlov et al.: Inaccurate estimation of biases in herbarium specimen data

Kozlov and colleagues1 call into question the application of herbarium specimens to quantify historical patterns of herbivory2-5. It is already widely appreciated that collectors of herbarium specimens may tend to avoid insect damage, thus making herbivory estimates from herbarium specimens potentially down-biased2. However, Kozlov et al. additionally suggest that variation in sampling selectivity among collectors and curators may lead herbarium specimens to misrepresent patterns of herbivory in nature. The authors sought to quantify these biases by collecting and contrasting insect herbivory data across 17 plant species from herbarium versus standard field ecological sampling procedures, and then assessed the selection of these specimens by curators. They concluded that herbivory estimates from herbarium specimens are highly variable, rendering them an inaccurate representation of herbivory in nature. Our re-analysis of Kozlov et al.s data suggests that, in contrast with their results, herbarium specimens indeed provide a useful record of herbivory as long as sample sizes are appropriate. In addition, we assert that by arguing that herbarium specimens are "distorting mirrors", Kozlov et al.s conclusions fundamentally overstep their data, which narrowly assesses biases across species. Kozlov et al. argue that herbarium specimens are inaccurate data sources, but fail to characterize the specific circumstances under which assumed biases would apply. Thus, Kozlov et al.s data do not support their main premise, and the authors extrapolate beyond the specific biases investigated in their study; we believe their contribution does a disservice to researchers interested in exploring the potential value of herbarium specimens for studying herbivory through time.

ecology↗

Phenological displacement is uncommon among sympatric angiosperms

Interactions between species can influence access to resources and successful reproduction. One possible outcome of such interactions is reproductive character displacement. Here, the similarity of reproductive traits - such as flowering time - among close relatives growing in sympatry differ more so than when growing apart. However, evidence for the overall prevalence and direction of this phenomenon, or the stability of such differences under environmental change, remains untested across large taxonomic and spatial scales. We apply data from tens of thousands of herbarium specimens to examine character displacement in flowering time across 110 animal-pollinated angiosperm species in the eastern USA. We demonstrate that the degree and direction of phenological displacement among co-occurring closely related species pairs varies tremendously. Overall, flowering time displacement in sympatry is not common. However, displacement is generally greater among species pairs that flower close in time, regardless of direction. We additionally identify that future climate change may alter the nature of phenological displacement among many of these species pairs. On average, flowering times of closely related species were predicted to shift further apart by the mid-21st century, which may have significant future consequences for species interactions and gene flow.

ecology↗

Water lily (Nymphaea thermarum) draft genome reveals variable genomic signatures of ancient vascular cambium losses

For more than 225 million years, all seed plants were woody trees, shrubs, or vines (1-4). Shortly after the origin of angiosperms ~135 million years ago (MYA) (5), the Nymphaeales (water lilies) became one of the first lineages to deviate from their ancestral, woody habit by losing the vascular cambium (6), the meristematic population of cells that produces secondary xylem (wood) and phloem. Many of the genes and gene families that regulate differentiation of secondary tissues also regulate the differentiation of primary xylem and phloem (7-9), which are produced by apical meristems and retained in nearly all seed plants. Here we sequence and assemble a draft genome of the water lily Nymphaea thermarum, an emerging system for the study of early flowering plant evolution, and compare it to genomes from other cambium-bearing and cambium-less lineages (like monocots and Nelumbo). This reveals lineage-specific patterns of gene loss and divergence. Nymphaea is characterized by a significant contraction of the HD-ZIP III transcription factors, specifically loss of REVOLUTA, which influences cambial activity in other angiosperms. We also find the Nymphaea and monocot copies of cambium-associated CLE signaling peptides display unique substitutions at otherwise highly conserved amino acids. Nelumbo displays no obvious divergence in cambium-associated genes. The divergent genomic signatures of convergent vascular cambium loss reveals that even pleiotropic genes can exhibit unique divergence patterns in association with independent trait loss events. Our results shed light on the evolution of herbaceousness - one of the key biological innovations associated with the earliest phases of angiosperm evolution. Significance StatementFor ~225 million years, all seed plants were woody trees, shrubs, or vines. Shortly after the origin of flowering plants ~135 million years ago, Nymphaeales (water lilies) became one of the first seed plant lineages to become herbaceous through loss of the meristematic cell population known as the vascular cambium. We sequence and assemble the draft genome of the water lily Nymphaea thermarum, and compare it to genomes of other plants that have retained or lost the vascular cambium. By using both genome-wide and candidate-gene analysis, we find lineage-specific patterns of gene loss and divergence associated with cambium loss. Our reveal divergent genomic signatures of convergent trait loss in a system characterized by complex gene-trait relationships.

plant biology↗

Freezing and water availability structure the evolutionary diversity of trees across the Americas

The historical course of evolutionary diversification shapes the current distribution of biodiversity, but the main forces constraining diversification are unclear. We unveil the evolutionary structure of tree species diversity across the Americas to assess whether an inability to move (dispersal limitation) or to evolve (niche conservatism) is the predominant constraint in plant diversification and biogeography. We find a fundamental divide in tree lineage composition between tropical and extratropical environments, defined by the absence versus presence of freezing temperatures. Within the Neotropics, we uncover a further evolutionary split between moist and dry forests. Our results demonstrate that American tree lineages, though broadly distributed geographically, tend to retain their ancestral environmental relationships and that phylogenetic niche conservatism is the primary force structuring the distribution of tree biodiversity.

ecology↗

The unrealized potential of herbaria in global change biology

Plant and fungal specimens in herbaria are becoming primary resources for investigating how plant phenology and geographic distributions shift with climate change, greatly expanding inferences across spatial, temporal, and phylogenetic dimensions. However, these specimens contain a wealth of additional data--including nutrients, defensive compounds, herbivore damage, disease lesions, and signatures of physiological processes--that capture ecological and evolutionary responses to the Anthropocene but which are less frequently utilized. Here, we outline the diversity of herbarium data, global change topics to which they have been applied, and new hypotheses they could inform. We find that herbarium data have been used extensively to study impacts of climate change and invasive species, but that such data are less commonly used to address other drivers of biodiversity loss, including habitat conversion, pollution, and overexploitation. In addition, we note that fungal specimens are under-explored relative to vascular plants. To facilitate broader application of plant and fungal specimens in global change research, we outline the limitations of these data and modern sampling and statistical tools that may be applied to surmount challenges they present. Using a case study of insect herbivory, we illustrate how novel herbarium data may be employed to test hypotheses for which few data exist, despite potentially large biases. With the goal of positioning herbaria as hubs for global change research, we suggest future research directions and curation priorities.

plant biology↗

Widespread ancient whole genome duplications in Malpighiales coincide with Eocene global climatic upheaval

Ancient whole genome duplications (WGDs) are important in eukaryotic genome evolution, and are especially prominent in plants. Recent genomic studies from large vascular plant clades, including ferns, gymnosperms, and angiosperms suggest that WGDs may represent a crucial mode of speciation. Moreover, numerous WGDs have been dated to events coinciding with major episodes of global and climatic upheaval, including the mass extinction at the KT boundary (~65 Ma) and during more recent intervals of global aridification in the Miocene (~10-5 Ma). These findings have led to the hypothesis that polyploidization may buffer lineages against the negative consequences of such disruptions. Here, we explore WGDs in the large, and diverse flowering plant clade Malpighiales using a combination of transcriptomes and complete genomes from 42 species. We conservatively identify 22 ancient WGDs, widely distributed across Malpighiales subclades. Our results provide strong support for the hypothesis that WGD is an important mode of speciation in plants. Importantly, we also identify that these events are clustered around the Eocene-Paleocene Transition (~54 Ma), during which time the planet was warmer and wetter than any period in the Cenozoic. These results establish that the Eocene Climate Optimum represents another, previously unrecognized, period of prolific WGDs in plants, and lends support to the hypothesis that polyploidization promotes adaptation and enhances plant survival during major episodes of global change. Malpighiales, in particular, may have been particularly influenced by these events given their predominance in the tropics where Eocene warming likely had profound impacts owing to the relatively tight thermal tolerances of tropical organisms.\n\nSignificance StatementWhole genome duplications (WGDs) are hypothesized to generate adaptive variations during episodes of climate change and global upheaval. Using large-scale phylogenomic assessments, we identify an impressive 22 ancient WGDs in the large, tropical flowering plant clade Malpighiales. This supports growing evidence that ancient WGDs are far more common than has been thought. Additionally, we identify that WGDs are clustered during a narrow window of time, ~54 Ma, when the climate was warmer and more humid than during any period in the last ~65 Ma. This lends support to the hypothesis that WGDs are associated with surviving climatic upheavals, especially for tropical organisms like Malpighiales, which have tight thermal tolerances.

evolutionary biology↗

Widespread sampling biases in herbaria revealed from large-scale digitization

O_LINon-random collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras offer a timely opportunity to assess commonalities and differences in herbarium sampling biases.\nC_LIO_LIWe determined spatial, temporal, trait, phylogenetic, and collector biases in [~]5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England (NE).\nC_LIO_LIWe identified numerous shared and unique biases among these regions. Shared biases included specimens i) collected close to roads and herbaria; ii) collected more frequently during spring; iii) of threatened species collected less frequently; and iv) of close relatives collected in similar numbers. Regional differences included i) over-representation of graminoids in SA and AU and of annuals in AU; and ii) peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by a few individuals. These mega-collectors, and their associated preferences and idiosyncrasies, may have shaped patterns of collection bias via founder effects.\nC_LIO_LIStudies using herbarium collections should account for sampling biases and future collecting efforts should avoid compounding these biases.\nC_LI

plant biology↗